Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum
- McGill University, Canada
- Johns Hopkins University, United States
Abstract
The ability to accurately control our posture and perceive spatial orientation during self-motion requires knowledge of the motion of both the head and body. However, whereas the vestibular sensors and nuclei directly encode head motion, no sensors directly encode body motion. Instead, the integration of vestibular and neck proprioceptive inputs is necessary to transform vestibular information into the body-centric reference frame required for postural control. The anterior vermis of the cerebellum is thought to play a key role in this transformation, yet how its Purkinje cells integrate these inputs or what information they dynamically encode during self-motion remains unknown. Here we recorded the activity of individual anterior vermis Purkinje cells in alert monkeys during passively applied whole-body, body-under-head, and head-on-body rotations. Most neurons dynamically encoded an intermediate representation of self-motion between head and body motion. Notably, these neurons responded to both vestibular and neck proprioceptive stimulation and showed considerable heterogeneity in their response dynamics. Furthermore, their vestibular responses demonstrated tuning in response to changes in head-on-body position. In contrast, a small remaining percentage of neurons sensitive only to vestibular stimulation unambiguously encoded head-in-space motion across conditions. Using a simple population model, we establish that combining responses from ~40-50 Purkinje cells can explain the responses of their target neurons in deep cerebellar nuclei across all self-motion conditions. We propose that the observed heterogeneity in Purkinje cells underlies the cerebellum's capacity to compute the dynamic representation of body motion required to ensure accurate postural control and perceptual stability in our daily lives.
Data availability
All data and codes to generate figures are available on Figshare under the URL: https://doi.org/10.6084/m9.figshare.19362239
Article and author information
Author details
Funding
National Institute on Deafness and Other Communication Disorders (R01-DC002390)
- Kathleen E Cullen
National Institute on Deafness and Other Communication Disorders (R01-DC018061)
- Kathleen E Cullen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All experimental protocols were approved by the Johns Hopkins University Animal Care and Use Committee and were in compliance with the guidelines of the United States National of Health.(PR19M408)
Copyright
© 2022, Zobeiri & Cullen
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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